The European anchovy (Engraulis encrasicolus ) increase in the North Sea Kristina Raab Thesis committee Promotor Prof. Dr Adriaan D. Rijnsdorp, Professor of Sustainable Fisheries Management Wageningen University Co-promotors Dr Mark Dickey-Collas Professional Officer, International Council for the Exploration of the Sea (ICES) Copenhagen, Denmark Dr Leo A.J. Nagelkerke Assistant professor, Aquaculture and Fisheries Group Wageningen University Other members Prof. Dr Brian MacKenzie, Technical University of Denmark, Institute for Aquatic Resources (DTU AQUA), Charlottenlund, Denmark Prof. Dr Jaap van der Meer, Royal Netherlands Institute for Sea Research (NIOZ), Texel, The Netherlands Prof. Dr Wolf M. Mooij, Wageningen University and Netherlands Institute for Ecology (NIOO), Wageningen Dr W. Fred de Boer, Wageningen University This research was conducted under the auspices of the Graduate School of Animal Sciences. The European anchovy (Engraulis encrasicolus ) increase in the North Sea Kristina Raab Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof.dr M.J. Kropff, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Thursday 10 October 2013 at 11 a.m. in the Aula. Kristina Raab The European anchovy ( Engraulis encrasicolus) increase in the North Sea, 208 pages. PhD thesis, Wageningen University, Wageningen, NL (2013) With references, with summaries in Dutch and English ISBN 978 94 6173 6826 “In liebevoller Verehrung”… To my teachers, past and present. Contents Chapter 1 - General introduction.......................................................... 9 Chapter 2 - Anchovy Engraulis encrasicolus diet in the North and Baltic Seas (Raab et al 2011).................................................................. 37 Chapter 3 - Dietary overlap between the potential competitors herring, sprat and anchovy in the North Sea (Raab et al 2012)………….. 67 Chapter 4 - Anchovy population expansion in the North Sea (Petitgas et al 2012)………………………………………………………………………………………... 91 Chapter 5 - Impact of temperature and food availability on juvenile European anchovy ( Engraulis encrasicolus ) at its northern boundary (Raab et al 2013)…………………………………………………………………………….... 115 Chapter 6 - Depensation in small pelagic fish illustrated with the North Sea anchovy example (manuscript) ……………………………..………... 141 Chapter 7 - Synthesis and general discussion…………………………….…….. 169 English Summary ……………………………………………………………………………… 193 Dutch Summary (Samenvatting) …………………………………………………...... 196 Acknowledgements …………………………………………………………………………. 199 About the author …………………………………………………………………………….. 205 List of publications …………………………………………………........................... 207 CHAPTER 1 Introduction: A background review for the anchovy increase in the North Sea 9 Small pelagic fish populations, i.e. planktivorous schooling fish, mainly of the order Clupeiformes, are of global importance both socio-economically and ecologically (Pikitch et al. 2012a, Pikitch et al. 2012b). In the North Sea, herring and sprat are important species in terms of number and fishery (Dickey-Collas et al. in press). European anchovy ( Engraulis encrasicolus ) is usually found further South in Europe: in the Bay of Biscay, Mediterranean and Black Seas (Barange et al. 2009) but also in small numbers on the southern coast of the North Sea (Boddeke & Vingerhoed 1996). In the mid-1990s, anchovy in the North Sea showed an increase in abundance and distribution as far North as Scotland (Beare et al. 2004). The reasons for this increase were unknown, but changes in this population may reflect or indicate changes in other components of the North Sea ecosystem. Indeed, many concurrent changes were happening in the North Sea. Among these, changes in the plankton and general warming due to climate change appeared likely to influence this planktivorous fish previously found further South in Europe. This thesis therefore addresses the ecology of anchovy in the North Sea, including possible causes and mechanisms for the anchovy increase. First by establishing basic trophic and life cycle characteristics of anchovy, then by focusing on the impact of environmental variables like food availability and temperature on young anchovy and lastly by generalising to possible spatial range expansion processes. This introductory chapter gives an overview of the main background to the thesis and outlines the questions, hypotheses and approaches we use. The importance of small pelagic fish in global ecosystems is presented, as well as further details on the North Sea anchovy and its population increase. I then give an overview of important processes regulating population dynamics, relating these to changes observed in the North Sea. The importance of space and scale in ecology is noted and we briefly explain the implications for the concept of regime shifts in the oceans. Small pelagic fish in a global perspective The economic importance of small pelagic fish results from the magnitude of the catches of these fish across several major oceans, rather than from a high value of the fish per se . Indeed, the catches make up over 50% of the world’s wild- caught catches despite coming from only 3.7% of all recorded fish species (Cury et al. 2000). Ecologically, small pelagic fish play a crucial role because they can constitute such a large biomass in pelagic systems that they have the capacity to exert strong bottom up or top down control. Bottom up control is the type of ecological control where resource availability controls consumer/predator 10 INTRODUCTION ǀ CHAPTER 1 populations – e.g. the small pelagics supporting large populations of carnivorous fish, seabirds and marine mammals. However, these small pelagics may also exert top-down control, where resource populations are controlled by a predator, e.g. they might be limiting the populations of the plankton species they feed on (e.g. mesocosm experiments by Mowitt et al. 2006 and suggested in e.g. the Baltic by Casini et al. 2006). The extent to which bottom up and top down control plays a role in ecological systems and in marine systems specifically has been heavily debated. Generally systems were thought of as being controlled either in a bottom up/resource-limited or a top down/predation-controlled way, but then the example of small pelagics opened a way to a more diversified way of considering the ecological control mechanisms. Small pelagics were singled out as so-called “wasp-waist” control species (Rice 1995, Cury et al. 2000, Bakun 2006), controlling the higher trophic levels by bottom up control and the lower trophic levels by top down control. This makes them a pivotal component of the system, possibly in the North Sea as well (Fauchald et al. 2011), although recent analyses suggest the wasp-waist idea in general may be an oversimplification (Fréon et al. 2009, Madigan et al. 2012). An interesting feature of small pelagic fish populations is that they naturally undergo large-scale abundance fluctuations associated with range changes on a regular basis (Lluch-Belda et al. 1989, Schwartzlose et al. 1999, Lehodey P. et al. 2006). Sometimes, species pairs in a same system alternate in their dominance by biomass, e.g. anchovy and sardine in the Benguela, Humboldt, California and Japan systems (reviewed by Schwartzlose et al. 1999 or sardine and herring in the English Channel Alheit & Hagen 1997). Nowadays and historically however, fluctuations in species abundance do not always correspond to species alternations (Soutar & Isaacs 1974). Climate was long considered to be the main driver behind these abundance fluctuations, although the possible impact of other factors such as fishing has not been excluded (fishing has been invoked as possible cause for large-scale declines of fish populations e.g. Hutchings & Myers 1994, Jackson et al 2001, Roberts 2007). Support for the climate theory comes from the close correspondence between population abundance and climate conditions e.g. in the North Pacific for instance, sardine dominates under warm conditions, while in cold phases, anchovy prevails (Lluch-Belda et al. 1989). Moreover, there is a correspondence of phase timings across different ocean basins, with pelagic stocks fluctuating in phase with each other (e.g. Northwest and Southeast Pacific sardine) which resulted in the suggestion that long distance climatic linkages may be involved. There are however some exceptions such as e.g. the Californian sardine stock which is out of phase with the others (Schwartzlose et al. 1999). Yet since climate cannot be controlled for in large-scale marine systems, progress is largely made by the comparative rather than experimental method, which makes advances slow as there 11 are many case studies to bring under one consistent framework. It should be noted that even if the climate hypothesis is correct and climate were the ultimate cause of fluctuations, the proximate mechanisms remain unknown. Mechanisms proposed include that the species alternations are trophodynamically mediated (van der Lingen et al. 2006) with one species benefitting from slight changes in plankton availability, or related to the species having different optimal temperatures for growth (Takasuka et al. 2007) or differential abilities to evade biological controls (loophole concept, Bakun & Broad 2003) but consensus has not yet emerged. A recent synthesis (MacCall 2009) tries to bridge between climate behaviour and other factors